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Mitogen-activated protein kinase activity and microtuble organisation are altered by protein synthesis inhibition in maturing porcine oocytes

  • Maki Inoue (a1), Kunihiko Naito (a1), Taisuke Nakayama (a1) and Eimei Sato (a1)

Summary

Previously we have shown that mitogen-activated protein (MAP) kinase activity abruptly increases at the first metaphase (M1) and remains significantly higher than that at the germinal vesicle (GV) stage until the second metaphase (M2) in porcine oocytes cultured in vitro. The present paper describes how the mechanism of the blockage of meiotic maturation by protein sythesis inhibition involves MAP kinase regulation. Cycloheximide arrested both germinal vesicle breakdown (GVBD) and the normal transition from M1 to M2. MAP kinase activation was also reduced in these maturation-inhibited oocytes. By using immunofluorescence microscopy with the monoclonal antibody raised against rat α-tubulin, we showed that cycloheximide caused morphological abnormality in a spindle at M1, but not at M2. All these results indicate that in porcine oocytes: (1) GV blockage by protein synthesis inhibition involves the suppression of both histone H1 kinase and MAP kinase activation, (2) during the transition from M1 to M2, maintenance of a normal metaphasic spindle and high MAP kinase activity require protein synthesis, and (3) once the M2 cytoskeletal structures have been completed, and/or after the ‘critical period’, cytostatic factor activity is independent of protein synthesis.

Copyright

Corresponding author

M.Inoue, Department of Reproductive and Developmental Biology, The Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, 108Japan. Telephone: +81-3-5449-5753. Fax: +81-3-5449-5455. e-mail: ban@ims.u-tokyo.ac.jp.

References

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Davis, R.J. (1993). The mitogen-activated protein kinase signal transduction pathway. Biol. Chem. 268, 14553–6.
Downs, S.M. (1989). Specificity of epidermal growth factor action on maturation of the murine oocyte and cumulus oophorus in vitro. Biol. Reprod. 41, 371–9.
Gille, H., Sharrocks, A.D. & Shaw, P.E. (1992). Phosphorylation of transcription factor p62TCF by MAP kinase stimulates ternary complex formation at c-fos promoter. Nature. 358, 414–17.
Gotoh, Y., Nishida, E., Matsuda, S., Shiina, N., Kosako, H., Shiokawa, K., Akiyama, T., Ohta, K. & Sakai, H. (1991). in vitro effect on microtubule dynamics of purified Xenopus M phase-activated MAP kinase. Nature. 349, 251–4.
Hashimoto, N. & Kishimoto, T. (1988). Regulation of meiotic metaphase by a cytoplasmic maturation promoting factor during mouse oocyte maturation. Dev. Biol. 126, 242–52.
Inoue, M., Naito, K., Aoki, F.Toyoda, Y. & Sato, E. (1995). Activation of mitogen-activated protein kinase during meioteic maturation in porcine oocytes Zygote. 3 265–71.
Jung, Y., Fulka, J. Jr, Lee, C. & Moor, R.M. (1993). Effects of the protein phoshorylation inhibitor genistein on maturation of pig oocytes in vitro. J. Reprod. Fertil. 98, 529–35.
Kosako, H., Gotoh, Y., Matsuda, S., Ishikawa, M. & Nishida, E. (1992). Xenopus MAP Kinase activator is a serine/tyrosine kinase activated by threonine phosphorylation. EMBo J. 11, 2903–8.
Kosako, H., Gotoh, Y. & Nishida, E. (1994 a). Requirement for the MAP kinase kinase/map kinase cascade in Xenopus oocyte maturation. EMBO J. 13, 2131–8.
Kosaka, H., Gotoh, Y. & Nishida, E. (1994b). Mitogenactivated protein kinase kinase is required for the Mosinduced metaphase atttest. J. Biol. Chem. 269, 28354–8.
Kubelka, M., Motlik, J. Jr, Prochazka, R., Rimkevicova, Z. & Fulka, J. (1988). Time sequence of germinal vesicle breakdown in pig oocytes after cycloheximide and p-aminobenzamidine block. Gamete Res. 19, 423–31.
Kubelka, M., Rimkevicova, Z., Guerrier, P. & Motlik, J. (1995). Inhibition of protein synthesis affects histone H1 kinase, but not chromosome condensation activity, during the first meiotic division of pig oocytes. Mol. Reprod. Dev. 41, 63–9.
Laemmli, U. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227, 680–5.
Le Gal, F., Gall, L. & DeSmedt, V. (1992). Changes in protein synthesis pattern during in vitro maturation of goat oocytes. Mol. Reprod. Dev. 32, 18.
Matsuda, S., Kosako, H., Takenaka, K., Moriyama, K., Sekai, H., Akiyama, T., Gotoh, Y. & Nishida, E. (1992). Xenopus MAP kinase activator: identification and function as a key intermediate in the phosphorylation cascade. EMDO J. 11, 973–82.
Matsuda, S., Gotoh, Y. & Nishida, E. (1993). Phosphorylation of Xenopus mitogen-activated protein (MAP) kinase kinase by MAP kinase kinase kinase and MAP kinase. J. Biol. Chem. 268, 3277–81.
Moor, R.M. & Crosby, I.M. (1986). Protein requirements for germinal vesicle breakdown in ovine oocytes. J. Embryol. Exp. Morphol. 94, 207–20.
Motlik, J. & Rimekevicova, Z. (1990). Combined effects of protein synthesis and phosphorylation inhibitors on maturation of mouse oocytes in vitro. Mol. Reprod. Dev. 27, 230–4.
Naito, K. & Toyoda, Y. (1991). Fluctuation of histone H1 kinase activity during meiotic maturation in porcine oocytes. J. Reprod. Fertil. 93. 467–73.
Naito, K., Fukuda, Y. & Toyoda, Y. (1988). Effects of porcine follicular fluid on male pronucleus formation in porcine oocytes matured in vitro. Gamete Res. 21, 289–95.
Naito, E., Hawkins, C., Yamashita, R.M. (1995). Assocition of p34cdc2 and cyclin B1 during meiotic maturation in pig oocytes. Dev. Biol. 168, 627–34.
Nishida, E. & Gotoh, Y. (1993). The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem. Sci. 18, 128–31.
Nurse, P. (1990). Universal control mechanism regulating onset of M-phase. Nature. 344, 503–8.
Posada, J. & Cooper, J.A. (1992). Requirements for phosphorylation of MAP kinase during meiosis in Xenopus oocytes. Science. 255, 212–15.
Posada, J.Sanghera, J., Pelech, S., Aebersold, R. & Cooper, J.A. (1991). Tyrosine phosphorylation and activation of homologous protein kinases during oocyte maturation and mitogenic activation of fibroblasts. Mol. Cell Biol. 11, 2517–28.
Sagata, N., Daar, I., Oskarsson, M., Showalter, S.D.Vande Woude, G.F. (1989). The product of the mos proto-oncogene as a candidate ‘initiator’ for oocyte maturation. Science. 245, 643–6.
Sanghera, J.S., McNabb, C.K., Tonks, N. & Pelech, S.L. (1991). Tyrosyl phosphorylation and activation of the myelin basic protein kinase p44mpk during sea star oocyte maturation. Biochim. Biophys. Acta. 1095, 153–60.
Shibuya, E.K., Boulton, T.G., Cobb, M.H. & Ruderman, J.V. (1992). Activation of p42 map kinase and the release of oocytes from cell cycle arrest. EMBO J. 11, 3963–75.
Sobajima, T., Aoki, F. & Kohmoto, K. (1993). Activation of mitogen-activated protein kinase during meiotic maturation in mouse oocytes. J. Reprod.Fertil. 97, 389–94.
Sturgill, T.W., Ray, L.B., Erikson, E. & Maller, J.L. (1988). Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II. Nature. 334, 715–18.
Szollosi, M.S., Kubiak, J., Debey, P., De, Pennart H & Szollosi, D. (1993). Inhibiton of kinases by 6-dimethylaminopurine accelerates the transition to interphase in activated mouse oocytes. J.Cell Sci. 104, 861–72.
Tatemoto, H. & Horiuchi, T. (1995). Requirements for protein synthesis during the onset of meiosis in bovine oocytes and its involvement in the autocatalytic amplification of maturation-promoting factor. Mol. Reprod. Dev. 41, 4753.
Toyoda, Y., Yokoyama, M. & Hosi, T. (1971). Studies on the fertilization of mouse eggs in vitro. I. In vitro fertilization of eggs by fresh epididymal sperm. Jpn. Anim. Reprod. 16, 147–51.
Verlhac, M.H., Pennart, H., Maro, B., Cobb, M.H. & Clarke, H.J. (1993). MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev. Biol. 158, 330–40.
Verlhac, M.H., kubiak, J.Z., Clarke, H.J. & Maro, B., (1994). Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development. 120, 1017–25.
Verlhac, M.H., kubiak, J.Z., Weber, M., Geraud, G., Colledge, W.H., Evans, M.J. & Maro, B. (1996). Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development. 122, 815–22.
Yamauchi, N., Sasada, H. & Sugawara, S. (1995). Protein synthesis in porcine follicular oocytes during in vitro meiotic maturation. J. Mamm. Ova Res. 12, 5963.

Keywords

Mitogen-activated protein kinase activity and microtuble organisation are altered by protein synthesis inhibition in maturing porcine oocytes

  • Maki Inoue (a1), Kunihiko Naito (a1), Taisuke Nakayama (a1) and Eimei Sato (a1)

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